Abstract
A lichen is a composite organism formed of algae or cyanobacteria that live in a mutually advantageous symbiotic relationship with the filaments (hyphae) of fungus. Three lichen samples were obtained from diverse sites at a terrestrial habitat located in Coimbatore and coastal habitats located in Kanyakumari and Nagapattinam districts of Tamil Nadu. Amplification and sequencing of 16S rRNA V3–V4 regions were used for metagenomic study. Aside from the Next-Generation Sequencing data (NGS), distinct types of lichen microbiome profiles were clearly revealed. The bacterial diversity in the lichen genera of Roccella montagnei growing in coastal and terrestrial environments was further investigated using common and unique operational taxonomic units (OTUs) and the QIIME pipeline (1.9.1). Using similarity clustering, the heat map analysis depicts the abundance information of chosen OTUs as well as the similarity and difference between OTUs and lichen samples. Using multiple methods, the alpha and beta diversity analysis revealed that there were differences in all of the samples. However, UPGMA tree inference of comparable bacterial community in coastal habitat lichen samples compared to terrestrial habitat validates their evolutionary lineage. As a result, the bacterial population associated with corticolous lichen is dependent on geographic locations, growth substrate, and climatic circumstances of similar lichen genera produced in different habitats and tree substrates.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Almendras K, Garcia J, Caru M, Orlando J (2018) Nitrogen-fixing bacteria associated with Peltigera Cyanolichens and Cladonia Chlorolichens. Molecules 23(12):3077
Arnold AE, Miadlikowska J, Higgins KL, Sarvate SD, Gugger P, Way A, Hofstetter V, Kauff F, Lutzoni F (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Syst Biol 58:283–297
Aschenbrenner IA, Cardinale M, Berg G, Grube M (2014) Microbial cargo: do bacteria on symbiotic propagules reinforce the microbiome of lichens? Environ Microbiol 16(12):3743–3752
Aschenbrenner IA, Cernava T, Erlacher A, Berg G, Grube M (2017) Differential sharing and distinct co-occurrence networks among spatially close bacterial microbiota of bark, mosses and lichens. Mol Ecol 26(10):2826–2838
Babilonia J, Conesa A, Casaburi G, Pereira C, Louyakis AS, Reid RP, Foster JS (2018) Comparative metagenomics provides insight into the ecosystem functioning of the Shark Bay stromatolites Western Australia. Front Microbiol 9:1359. https://doi.org/10.3389/fmicb.2018.01359
Bates ST, Cropsey GWG, Caporaso JG, Knight R, Fierer N (2011a) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314
Bates ST, Garrett WG, Cropsey JG, Caporaso RK, Fierer N (2011b) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77(4):1309–1314. https://doi.org/10.1128/AEM.02257-10
Beckett RP, Kranner I, Minibayeva FV (2008) Stress physiology and the symbiosis. In: Nash TH (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 134–151
Boddy L, Dyer PS, Helfer S (2010) Plant pests and perfect partners. In: Boddy L, Coleman M (eds) From another kingdom. Royal Botanic Gardens, Edinburgh, pp 52–65
Budel B, Scheidegger DC (2008) Thallus morphology and anatomy. In: Nash TH (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 40–68
Cardinale M et al (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71
Cardinale M, Steinova J, Rabensteiner J, Berg G, Grube M (2012) Age, sun and substrate: triggers of bacterial communities in lichens. Environ Microbiol Rep 4:23–28
Cernava T, Aschenbrenner IA, Grube M, Liebminger S, Berg G (2015a) A novel assay for the detection of bioactive volatiles evaluated by screening of lichen-associated bacteria. Front Microbiol 6:398. https://doi.org/10.3389/fmicb.2015.00398
Cernava T, Müller H, Aschenbrenner IA, Grube M, Berg G (2015b) Analyzing the antagonistic potential of the lichen microbiome against pathogens by bridging metagenomic with culture studies. Front Microbiol 6:620. https://doi.org/10.3389/fmicb.2015.00620
Cernava T, Erlacher A, Aschenbrenner IA, Krug L, Lassek C, Riedel K, Grube M, Berg G (2017) Deciphering functional diversification within the lichen microbiota by meta-omics. Microbiome 5:82. https://doi.org/10.1186/s40168-017-0303-5
Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, Ley RE (2014) Conducting a microbiome study. Cell 158(2):250–262
Graham LE, Trest MT, Will-Wolf S, Miicke NS, Atonio LM, Piotrowski MJ, Knack JJ (2018) Microscopic and metagenomic analyses of Peltigera ponojensis (Peltigerales, ascomycota). Int J Plant Sci 179(3):241–255
Grube M, Cardinale M, de Castro JV, Muller H, Berg G (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3(9):1105–1115
Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C et al (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424. https://doi.org/10.1038/ismej.2014.138
Hassan M, Essam T, Megahed S (2018) Illumina sequencing and assessment of new cost-efficient protocol for metagenomic-DNA extraction from environmental water samples. Braz J Microbiol 49S:1–8
Henkel PA, Plotnikova TT (1973) Nitrogen-fixing bacteria in lichens. Izv Akad Nauk Ser Biol 1973:807–813
Henkel PA, Yuzhakova LA (1936) Nitrogen-fixing bacteria in lichens. Izv Biol Inst Permsk Gos Univ 10:9–10
Hodkinson BP, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180
Hodkinson BP, Gottel NR, Schadt CW, Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161
Honegger R (1993) Tansley review No. 60. Developmental biology of lichens. New Phytol 125(4):659–677
Iskina RY (1938) On nitrogen fixing bacteria in lichens. Isv Biol Inst Permsk 11:133–139
Jahns HM (1973) Anatomy, morphology, and development. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 3–58
Lee YM, Kim EH, Lee HK, Hong SG (2014) Biodiversity and physiological characteristics of Antarctic and Arctic lichens-associated bacteria. World J Microbiol Biotechnol 30(10):2711–2721
Leiva D, Fernandez-Mendoza F, Acevedo J, Caru M, Grube M, Orlando J (2021) The bacterial community of the foliose macro-lichen Peltigera frigida is more than a mere extension of the microbiota of the subjacent substrate. Microb Ecol 81(4):965–976
Panosyan AK, Nikogosyan VG (1966) The presence of Azotobacter in lichens. Akad Nauk Armian SSR Biol Zhurn Armen 19:3–11
Park CH, Kim KM, Kim OS, Jeong G, Hong SG (2016) Bacterial communities in Antarctic lichens. Antarct Sci 28(6):455–461
Printzen C, Fernandez-Mendoza F, Muggia L, Berg G, Grube M (2012) Alphaproteobacterial communities in geographically distant populations of the lichen Cetraria aculeata. FEMS Microbiol Ecol 82(2):316–325
Sierra MA, Danko DC, Sandoval TA, Pishchany G, Moncada B, Kolter R, Mason CE, Zambrano MM (2020) The microbiomes of seven lichen genera reveal host specificity, a reduced core community and potential as source of antimicrobials. Front Microbiol 11(3):1–12 (398)
Sigurbjornsdottir MA, Vilhelmsson O (2016) Selective isolation of potentially phosphate-mobilizing, biosurfactant-producing and biodegradative bacteria associated with a sub-Arctic, terricolous lichen Peltigera membranacea. FEMS Microbiol Ecol 92:fiw090
Silva MAL, Medeiros Z, Soares CRP, da Silva ED, Miranda-Filho DB, de Melo FL (2014) A comparison of four DNA extraction protocols for the analysis of urine from patients with visceral leishmaniasis. Rev Soc Bras Med Trop 47(2):193–197
Solhaug KA, Gauslaa Y, Nybakken L, Bilger W (2003) UV-induction of sun-screening pigments in lichens. New Phytol 158(1):91–100
Thomas T, Gilbert J, Meyer F (2012) Metagenomics-a guide from sampling to data analysis. Microb Inf Exp 2(1):3–8
Uphof JT (1925) Purple bacteria as symbionts of a lichen. Science 61(1568):67–67
Acknowledgements
The first author thanks the Research Foundation of Bharathidasan University for the fellowship (URF) (021505/URF/DIR-RES/2019 Date: 22.10.2019). DST-FIST (Department of Science and Technology-Fund for improvement of S & T infrastructure), New Delhi, is express gratitude for the instrumentation facility (DST Sanction Order No.: SR/FIST/LSI-013/ 2012/Dt.13.08.2012). We acknowledge the financial assistance of the Department of Science and Technology, Government of India, under DST-Promotion of University Research and Scientific Excellence (PURSE) scheme—Phase II, Rashtriya Uchchatar Shiksha Abhiyan (RUSA)-2. O Biological Sciences (TN RUSA: 311/RUSA (2.0)/2018 dt. December 02, 2020) for facility to carry out the research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vijayakumar, V.R., Saravanan, K., Somasundaram, M. et al. Metagenomic analysis of lichen-associated bacterial community profiling in Roccella montagnei. Arch Microbiol 204, 54 (2022). https://doi.org/10.1007/s00203-021-02707-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-021-02707-7